The Gut Microbiome Causally Contributes to Interspecific Differences in Pesticide Sensitivity

Abstract

Explaining interspecific differences in pesticide sensitivity is key to increasing the predictive power of ecotoxicology. Besides species traits, the gut microbiome may provide an untested additional predictive factor since it often plays a role in host defense against stressors. Therefore, we investigated the gut microbiome's causal role in shaping differences in pesticide sensitivity between two congeneric damselfly species. After an antibiotic treatment, reciprocal gut microbiome transplants were performed between pesticide-sensitive Ischnura elegans and more tolerant Ischnura pumilio larvae, with donor larvae first preexposed to either chlorpyrifos or a solvent control to match the subsequent pesticide treatments of the recipients. The gut microbiome, determined by 16S rRNA gene amplicon sequencing, of both species included pesticide-degrading bacteria, but also showed shared and species-specific responses to the pesticide. Notably, the most pesticide-sensitive combination, with the highest pesticide-induced mortality, consisted of I. elegans larvae receiving I. elegans donor gut microbiota, whereas the least sensitive combination consisted of I. pumilio larvae receiving I. pumilio donor gut microbiota, whereby the pesticide did not increase larval mortality. The two mixed donor-recipient gut microbiome combinations resulted in an intermediate sensitivity. Remarkably, I. elegans recipient larvae experienced a lower chlorpyrifos-induced mortality when they received an I. pumilio donor gut microbiome than when they received their conspecific I. elegans donor gut microbiome. Our results provide, to our knowledge, the first proof-of-evidence that the gut microbiome causally contributes to species differences in pesticide sensitivity.